Vol. 31: 259–270, 2016 ENDANGERED SPECIES RESEARCH Published November 28 doi: 10.3354/esr00768 Endang Species Res

OPENPEN ACCESSCCESS A shift in foraging behaviour of beluga whales Delphinapterus leucas from the threatened population may reflect a changing Arctic food web

Cortney A. Watt1,2,*, Jack Orr2, Steven H. Ferguson1,2

1Department of Biological Sciences, University of Manitoba, Winnipeg, MB R3T 2N2, 2Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, MB R3T 2N6, Canada

ABSTRACT: Cumberland Sound, an inlet on , , Canada, is undergoing changes in sea ice cover, which is affecting the marine food web. A small population of beluga whales Delphina pterus leucas inhabits Cumberland Sound year round and this population is cur- rently listed as threatened. Relatively little is known about the foraging behaviour of these belugas, but we expected that food web changes, primarily an increased abundance of in the region, would have an impact on their diet and dive behaviour. We evaluated fatty acids in blubber sam- ples collected from subsistence-hunted belugas in Cumberland Sound from the 1980s to 2010, and analyzed satellite tag information from 7 belugas tagged in 2006 to 2008 to gain a better under- standing of their foraging behaviour. There was a change in the fatty acid profile of beluga blubber from the 1980s compared to the 1990s and 2000s. Specific fatty acids indicative of capelin and Arc- tic cod increased and decreased over time respectively, suggesting an increased consumption of capelin with a reduction in Arctic cod in summer in more recent years. Dive behaviour suggested different foraging tactics across seasons. Shallow short dives occurred in summer, which may indi- cate foraging on capelin, while deeper longer dives were made in autumn and winter, possibly indicating foraging on deeper prey such as Arctic cod and Greenland . Potentially, autumn and winter are important foraging seasons for belugas, amassing energy reserves as blubber and creating a possible competitive conflict for resource use between belugas and expanding commer- cial fisheries.

KEY WORDS: Diet · Fatty acids · Diving · Fisheries competition · Capelin · Arctic cod ·

INTRODUCTION of the sound, and in winter belugas move towards the mouth of Cumberland Sound (Richard & Stewart Cumberland Sound is an inlet on the east coast of 2008). Whales in this population have been listed as Baffin Island, Nunavut, Canada. This region is a bio- threatened by the Committee on the Status of Endan- logically productive area and is an important summer gered Wildlife in Canada (COSEWIC 2004) as a feeding area for many (Cobb 2011). Beluga result of low population numbers (759 to 1960 indi- whales Delphinapterus leucas are ubiquitous in the viduals) (DFO 2005, Richard 2013, Marcoux et al. Arctic, and there is a small population that inhabits 2016). It is estimated there were >5000 belugas in Cumberland Sound year round (Richard & Stewart this population prior to large commercial hunting 2008). Whales spend summer in the northwestern catches between 1920 and 1960, while subsistence part of Cumberland Sound, particularly in Clearwa- hunts with managed quotas have been in place since ter Fiord. In autumn, whales are located in the centre the early 1980s with hunts of <50 individuals per year

© C. A. Watt, S. H. Ferguson and Fisheries and Oceans Canada *Corresponding author: [email protected] 2016. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 260 Endang Species Res 31: 259–270, 2016

(Mitchell & Reeves 1981, DFO 2002). There are also decline may be a result of an increased reliance on concerns regarding boat noise and competition with capelin as a primary prey resource. This also corre- Greenland halibut Reinhardtius hippoglossoides fish- lates with evidence suggesting that capelin had low eries, a potential prey of beluga whales (Heide- abundance in Cumberland Sound in the early 2000s, Jørgensen & Teilmann 1994). but had substantially increased in abundance by Climate change is also having impacts on the food 2011 (Ulrich 2013). web in Cumberland Sound. A reduction in sea ice in Along with chemical techniques such as stable iso- the Arctic has resulted in a northward shift of subarc- tope and fatty acid analysis, diet can also be assessed tic species that can compete with and displace Arctic by evaluating dive behaviour. Determining the species (Perovich & Richter-Menge 2009, Tivy et al. depths to which whales are diving can provide an 2011, McKinney et al. 2012). For example, in north- idea of where in the water column they are foraging ern the incidence of capelin Mallotus and subsequently determine what common prey are villosus increased from the mid-1980s to the late available at those depths (Watt et al. 2015). No eval- 1990s, with a subsequent decrease in Arctic cod uation of dive behaviour with respect to bottom Boreo gadus saida (Gaston et al. 2003). Similarly, in bathymetry has been conducted on belugas from Cumberland Sound the food web has been changing Cumberland Sound; however, dive data from belu- and there has been an increase in capelin and a gas in other regions has been analyzed with respect reduction in Arctic cod (McKinney et al. 2012, Ulrich to bottom bathymetry. In the Canadian High Arctic, 2013). Specifically, capelin were absent in the stom- beluga whales have been tagged and researchers achs of Arctic char Salvelinus alpinus from the Cum- found characteristic deep dives to the bottom that berland Sound region in the early 2000s, but made they interpreted as foraging dives (Martin & Smith up the bulk of their diet in 2011, and char are known 1992, 1999, Martin et al. 1998). In Hudson Bay, 2 pop- to forage opportunistically, resulting in a diet that ulations of whales were found to have different dive reflects prey availability in their environment behaviour. One of the populations used the entire (Rikardsen et al. 2007, Ulrich 2013). These changes water column when close to shore but spent more will undoubtedly affect the diet and behaviour of the time close to the sea floor when offshore, while beluga whales inhabiting the region. another population seemed to use the entire water Beluga whales are considered to have a more column regardless of distance from shore (Bailleul et diverse diet than other Arctic cetaceans (Laidre et al. al. 2012). Other belugas tagged in Hudson Bay made 2008). Arctic cod B. saida tends to dominate diet for consistent dives to the bottom (Kingsley et al. 2001), belugas from the eastern Beaufort Sea (Loseto et al. suggesting foraging on prey in the benthos. In the 2009, Quakenbush et al. 2015) and the Canadian eastern , Citta et al. (2013) found no dif- High Arctic (Matley et al. 2015). Pacific herring Clu- ference in the depths to which beluga whales of dif- pea pallasii, tomcod Microgadus tomcod (Huntington ferent sexes or ages dove, and diving depths sug- & The Communities of Buckland, Elim, Koyuk, Point gested whales foraged primarily from 200 to 1000 m. Lay and Shaktoolik 1999), rainbow smelt Osmerus However, Hauser et al. (2015) did find differences in mordax, Arctic cod B. saida, and saffron cod Eleginus the diving behaviour of adult belugas versus imma- gracilis are common dietary items for different bel- ture whales from the eastern Chukchi Sea, with uga stocks from Alaska (Quakenbush et al. 2015), adults spending significantly more time at deeper while halibut R. hippoglossoides, shrimp Pandalus depths. Hauser et al. (2015) were also able to corre- borealis, and redfish marinus were found in late beluga dives to the distribution of Arctic cod and beluga stomachs from Greenland whales (Heide-Jør- found that whales significantly targeted depths (200 gensen & Teilmann 1994). Relatively little is known to 300 m) with maximum cod abundance. about diet from beluga whales in Cumberland Dive behaviour was investigated from 1998 to 1999 Sound, but fatty acid analysis on a small number of in a few beluga whales (n = 13) from Cumberland samples (n = 15) from 1983 to 1987 suggests that Arc- Sound (Heide-Jørgensen et al. 2001). Although the tic cod was prevalent in diet (Kelley et al. 2010). Sta- authors did not evaluate diving in relation to bottom ble isotope analysis on skin and muscle tissues from bathymetry, they did determine that belugas from Cumberland Sound belugas from 2000 to 2010 sug- Cumberland Sound spend less time at the surface at gests that diet consists primarily of Arctic cod and night compared to day, with a trend towards more capelin M. villosus (Marcoux et al. 2012). Marcoux et night dives, suggesting this may be an important al. (2012) also found a significant decline in δ15N val- time for foraging (Heide-Jørgensen et al. 2001). In ues from 1982 to 2009 and they suggested this addition, when compared to whales from other Watt et al.: diet and diving 261

regions in the Canadian High Arctic, Cumberland abdominal region was collected, frozen, and sent to Sound whales had higher dive rates and these rates the Freshwater Institute, Winnipeg, MB, where sam- did not seem to change seasonally, although only 4 ples were stored at −20°C. Blubber was subsampled tags recorded dive information in the winter and only from these larger cores; a cube of blubber from the for a short time (final transmission on 1 January 2000) deepest (closest to the muscle) and most interior por- (Heide-Jørgensen et al. 2001). There was annual tion of the core (which excluded all exterior blubber variability in dive rates for Cumberland Sound that may have been oxidized over time) was used for whales but this was based on a very small sample analysis. Animals were aged by counting growth size of whales tagged in only 2 yr (Heide-Jørgensen layer groups in an extracted tooth (n = 179), and all et al. 2001). No studies of recent dive behaviour for these animals were >1 yr of age (1–2 yr, n = 4; 3–5 yr, Cumberland Sound belugas have been conducted, n = 9; 5–7 yr, n = 17; and >7 yr, n = 149). We were and given the food web changes currently ongoing in unable to age 9 of the animals as no tooth was col- the region, comparing biomarkers and dive behav- lected, but we assume these were also >1 yr of age, iour is warranted. as larger animals are targeted by hunters. The objectives of our study were to evaluate long- term diet trends of beluga whales in Cumberland Sound using fatty acid analysis and to investigate Fatty acid analysis dive behaviour for whales in this region. With changes in the Cumberland Sound food web over the A 0.5 g subsection of blubber was extracted from as past 30 yr, most notably an increase in capelin abun- close to the muscle as the sample allowed, and used dance (McKinney et al. 2012, Ulrich 2013), we ex - for lipid extraction following Folch et al. (1957) and pected diet to have changed over this Budge et al (2006). Blubber was freeze-dried for 48 h time frame as belugas adapted to these changes. In before lipid extraction. Blubber was subjected to a particular, owing to the stable isotope evidence from chloroform:methanol solution (2:1) with 0.01% buty- belugas in Cumberland Sound that suggests a lated hydroxytoluene (BHT) and then removed, and decrease in δ15N and δ13C, which was hypothesized sodium chloride was added (3.5 ml). A dichloro - to represent an increased reliance on capelin from methane with 0.01% BHT and Hilditch (a mixture of 1982 to 2009 (Marcoux et al. 2012), as well as the evi- sulfuric acid and dry methanol) solution was then dence of increased capelin availability in Cumber- added, and fatty acid methyl esters (FAME) were land Sound, we hypothesized that belugas would produced by heating the sample for 1 h at 100°C. monopolize on this newly abundant prey source, Hexane, distilled water, and sodium sulfate were much like beluga whales in Hudson Bay have done added and then the sample was placed under an (Kelley et al. 2010). Through an understanding of evaporative nitrogen stream, and the total FAME diet changes and dive behaviour we can determine was weighted. Agilent Technologies 7890A GC sys- how belugas are responding to an increase in capelin tem was used to analyze the FAME sample. Stan- abundance in the region (McKinney et al. 2012, dards (Supelco 37 component FAME mix and Nu- Ulrich 2013), and evaluate the importance of differ- check 54 component mix GLC-463) were run every ent seasons for foraging. This is an important step for tenth sample, and FAME were identified by compar- understanding and conserving this threatened bel- ison to the standards and the resulting retention uga population. times. Many fatty acids are biosynthesized in predator tis- sues and are not informative for determining diet; MATERIALS AND METHODS thus, only 35 dietary fatty acids were evaluated in this study (Iverson et al. 2004). As a result of the Blubber collection detection limit of the gas chromatography, some indi- viduals are interpreted as having 0% of a given fatty Blubber samples were collected from adult beluga acid; in these cases, an arbitrary small number whales by hunters from Pangnirtung, Nunavut, in (0.00001) was added (Kenkel 2006). Percent fatty Cumberland Sound (65° 13’ N, 66° 45’ W) from 1984 acid values were divided by the percentage of the to 2010 (n = 188; 80 females and 108 males deter- reference fatty acid C18:0 and log transformed mined by genetic analyses). Whales were hunted op - (Budge et al. 2006). To calculate precision, 23 sam- por tunistically and were in good body condition (for ples were run in duplicate with an average standard consumption). A core of blubber tissue from the deviation of 0.04 ± 0.08% (average SD ± SD). 262 Endang Species Res 31: 259–270, 2016

A principal component analysis (PCA) of the 35 we were particularly interested in investigating dietary fatty acids was used to reduce the dimension- dietary shifts over time from Arctic cod to capelin, a ality of the log-transformed data to a few uncorrelated regression analysis with each fatty acid as a depend- dimensions, and the first 2 principal components ent variable and year as an independent variable was were used in further analysis. Principle components investigated. were then input into a multivariate analysis of vari- ance (MANOVA) to determine if beluga fatty acid values varied over time period (1980−1989, 1990− Dive behaviour 1999, and 2000−2010) or between sexes. Pillai’s trace was used to determine significance for each of the Satellite-linked time-depth recorder tags (SPLASH factors because it is considered the most powerful tags, Wildlife Computers) were deployed on adult and robust MANOVA statistic (Olson 1974). A canon- beluga whales to transmit daily information on their ical plot with scores obtained from a discriminant location and diving behaviour. A total of 7 belugas, 5 analysis on the principal components was used to females and 2 males, were tagged in Cumberland graphically display the multivariate fatty acid data. Sound (66° 16’ 18” N, 67° 05’ 90” W), near the com- Regression analysis was used to investigate how spe- munity of Pangnirtung, Nunavut, in July 2006 (n = 1), cific fatty acids changed over time. Although we did August 2007 (n = 2), and September 2008 (n = 4) not have a prey library to specifically compare bel- (Fig. 1, Table 1). Methods for beluga capture and tag- uga fatty acid signatures over time to those of poten- ging have previously been published (Orr et al. tial prey, there is evidence that whales in this popu- 2001). In short, belugas were captured in nets set lation forage primarily on capelin and Arctic cod perpendicular to the shore from a small island along (Marcoux et al. 2012), at least in the summer months. the migratory route of the whales on a daily basis, as Kelley et al. (2010) compared fatty acid signatures of weather permitted. Once caught, 2 inflatable zodiac capelin and Arctic cod using a PCA. The PCA identi- boats with at least 3 passengers would travel out to fied 5 dietary fatty acids representative of Arctic cod the net, pull the whale to the surface and hold it (20:1n7, 20:1n9, 22:1n9, 22:1n11, and 22:1n7) and 4 between the 2 boats for instrumentation with a satel- representative of capelin (18:2n6, 22:6n3, 22:5n6, and lite-linked transmitter. The whales were held in 20:4n6) (Kelley et al. 2010). t-tests confirmed that the place with a hoop net over the head, 3 to 4 straps fatty acids were significantly different between Arc- along their body, and a rubberized rope around the tic cod and capelin (p ≤ 0.001) (Kelley et al. 2010). As tailstock, which were all tied to loops on the boats.

Fig. 1. Tagging site (j) and the closest community, Pangnirtung, Nunavut (d), where beluga whales were tagged in 2006 to 2008, and the locations where Cumberland Sound belugas were diving >50 m in summer, autumn, and winter Watt et al.: Cumberland Sound beluga diet and diving 263

Table 1. Deployment date, sex, approximate length, the number of 6 h blocks for dive depth and dive duration collected, and the number of days dive information was transmitted for each season for beluga whales deployed with satellite-linked transmitters from 2006 to 2008 in Cumberland Sound. Dates given as mm/dd/yy

Deployment Sex Tag no. Length No. of 6 h blocks (dive depth/duration) Date of last dive Transmission date (cm) Summer Autumn Winter data transmission length (d)

07/18/06 F 57594 – 42/44 20/24 42/38 03/01/07 226 07/12/07 F 57602 350 104/110 8/13 0/0 10/29/07 109 07/12/07 F 37023 315 58/60 17/19 0/0 10/24/07 104 09/06/08 F 39296 290 45/48 14/32 50/79 05/09/09 246 09/05/08 F 39308 340 41/45 14/24 85/112 05/11/09 249 09/09/08 M 39323 370 48/50 18/34 72/66 04/18/09 222 09/09/08 M 40623 340 2/3 0/0 0/0 09/13/08 4

Three 10 mm nylon pins were then placed through provide dive information for 6 h increments every the dorsal ridge and the tag was anchored to the pins day from July to September, a time step of 6 h was with high-grade stainless steel wires looped around used to generate locations for this time period, while specially de signed washers. a time step of 4 d was used for transmission from The Argos system (CLS America) was used to ob - October to June. The International Bathymetric Chart tain location data. Locations were summarized into of the Arctic Ocean (IBCAO) provided shape files of four 6 h histograms, referred to from their starting ocean bathymetry with 500 m2 resolution (Jakobs son time, i.e. 02:00, 08:00, 14:00 and 20:00 h local time et al. 2012), which were projected using a North Pole at deployment location, every day throughout the projection in ArcGIS and were used to assign a depth months of July through September, and every fourth for each location (Fig. 1). day from October through June. All tags provided After bathymetry data was obtained for each loca- the mean number of dives belugas made to different tion, we isolated the dive depth bins that we were dive duration bins, and the number of dives to differ- interested in to evaluate foraging (>50 m deep). We ent depth bins for each 6 h period. The proportion of used deep diving as a proxy for marine mammal for- time spent in different depth bins was also collected, aging, as deep dives are often associated with prey but owing to the configurations of the tags, the maxi- capture (Davis et al. 2013). We assumed dives <10 m mum depth evaluated was 200 m and thus was not were associated with surface behaviours (Citta et al. particularly relevant for this study. The tags provide 2013) and that dives from the 10 to 50 m depth layer a depth resolution of 0.5 m (Wildlife Computers) and may represent transit or recovery diving (Hauser et all tags were programmed with the same bins; the al. 2015). In addition, although some foraging may number of dives to different depths were binned into occur at shallower depths, the main prey items for 6, 8, 10, 12, 15, 20, 25, 50, 100, 200, 300, 400, 500, and Cumberland Sound beluga whales determined by >500 m bins, and mean number of dives made to dif- stable isotope analysis are capelin and Arctic cod, ferent dive duration bins were binned into 60, 180, and adults of these species are typically found at 360, 540, 720, 900, 1080, 1260, 1440, and >1440 s bins depths >50 m (Falk-Petersen et al. 1986, Brown 2002, (Wildlife Computers). The accuracy of the transmis- Christiansen et al. 2012, Hauser et al. 2015) (see ‘Dis- sions was used to categorize the location information. cussion’ for further details). Depth bins representing Categories A and B provide no location information; dives deeper than 50 m were then converted to a per- Class 0 represents an error of >1500 m; Class 1, 500− centage of total depth for each location and grouped 1500 m; Class 2, 250−500 m; and Class 3, <250 m into different dive depth categories (Watt et al. 2015): (CLS America). dives that occurred in the upper 25% of total depth, Even when dive information was provided for the those that occurred from 26−50%, from 51−75% of previous 6 h, often the location associated with it was total water depth, and those dives that occurred in of low quality. As we wanted to use the location data the lower 76−100% of the total depth. There is uncer- to assign a depth to each dive, we needed a valid tainty in the depth estimates at these locations, and estimate of all locations. We generated locations because of this, dives sometimes exceeded the evenly spaced in time that considered the quality of IBCAO depths; in these cases, dives were included in the location from Argos using the Jonsen et al. (2005) the 76−100% category. The average depth at which estimation method. As the tags were programmed to whales were making dives >50 m did not vary signif- 264 Endang Species Res 31: 259–270, 2016

icantly across seasons. In summer, the average bathy- within each season as a random effect and season as metric depth at which whales were diving >50 m was a fixed factor was analyzed. When significant factors 247 m (range 75 to 652 m), compared to autumn, were identified, post-hoc Tukey’s HSD tests were when whales were in waters averaging 378 m depth used to determine where significant differences oc - (range 85 to 617m), and winter, where average depth cur red. R and JMP 9.0 software were used for all sta- was 230 m (range 77 to 581 m). tistical tests. Unfortunately, we did not have a large enough sam- ple size of males (n = 2, with 1 tag only lasting 7 d) to evaluate if different sexes have different dive behav- RESULTS iours. However, we did evaluate how the number of dives differed across seasons using repeated-mea- Fatty acid analysis sures ANOVAs. Seasons were defined based on previ- ous tracking data of beluga whales from Cumberland The first 2 principal components from the 35 Sound: July to September was identified as summer, dietary fatty acids explained 55% of the variability in October and November as autumn, and December to the data. A MANOVA on the first 2 principal compo- May as winter (Richard & Stewart 2008) (Fig. 1). One nents found no significant interaction between sexes model considered individual whales nested within and year category (F4,364 = 1.70, p = 0.15) or between each season as a random effect, and season (3 levels: sexes (F2,181 = 2.27, p = 0.11), but found a significant summer, autumn, and winter), depth (number of dives effect of time period (F4,364 = 3.40, p < 0.01) (Fig. 2). >50 m deep made to 0−25, 26−50, 51−75, and 76−100% Linear regression analysis of the 5 fatty acids repre- of total depth and 50−100, 100−200, 200−300, 300−400, sentative of Arctic cod revealed that from 1984 to 400−500, and >500 m), and the interaction between 2010 there was a downward trend for all fatty acids these factors as main effects (Underwood 1997). (20:1n7: y = −0.004x + 6.82, adjusted R2 = 0.00, SE = Repeated-measures ANOVA was also used to evalu- 0.30; 20:1n9: y = −0.01x + 17.40, adjusted R2 = 0.01, atedivedurationwhereindividualwhaleswerenested SE = 0.35; 22:1n7: y = −0.02x + 38.98, adjusted R2 = within each season as a random effect, and season (3 0.06, SE = 0.47; 22:1n9: y = −0.02x + 33.61, adjusted levels: summer, autumn, and winter), dive duration R2 = 0.06, SE = 0.39; 22:1n11: y = −0.01x + 29.77, (60, 180, 360, 540, 720, 900, 1080, 1260, 1440, and adjusted R2 = 0.05, SE = 0.37), and this trend was sig-

>1440 s), and the interaction between these factors as nificant for 3 of the fatty acids (22:1n9: F1,186 = 12.85, main effects (Underwood 1997). p < 0.001; 22:1n11: F1,186 = 9.87, p < 0.01; 22:1n7: Normality was assessed with normal probability F1,186 = 12.98, p < 0.001) (Fig. 3). Regression analysis plots, and a Box-Cox transformation was used on on the 4 dietary fatty acids representative of capelin dive depth and duration data to improve normality (Box & Cox 1964). The Mauchly 1980–1989 1990–1999 2000–2010 criterion (Mauchly 1940) was used to 0.2 1980–1989 Centroid 1990–1999 Centroid 2000–2010 Centroid assess sphericity and, when the spheric- 0.15 ity assumption was violated, adjusted Greenhouse-Geisser degrees of freedom 0.1 were used. This adjustment multiplies the calculated epsilon by the original degrees 0.05 of freedom to create a more conservative 0 test (Greenhouse & Geisser 1959). Depth CA1 and dive duration were considered –0.05 repeated-measures factors because bins were not independent of one another, –0.1 and the nested nature of the design accounted for within-subject variability –0.15 (Underwood 1997). When a significant –0.2 interaction was found in the main effects –0.25 –0.2 –0.15 –0.1 –0.05 0 0.05 0.1 0.15 0.2 model (described above) between season CA2 and depth/ dive duration, a simple effects Fig. 2. Canonical plot of beluga fatty acids from 3 time periods, 1980−1989 model for each depth/dive duration cate- (number of whales sampled = 38), 1990−1999 (n = 119), and 2000−2010 (n = gory with individual whales nested 31). Centroids ± SE are plotted for each time period Watt et al.: Cumberland Sound beluga diet and diving 265

found a positive trend for all fatty acids 3 20:1n9 20:1n7 (22:6n3: y = 0.02x − 31.10, adjusted R2 = 22:1n11* 0.02, SE = 0.51; 18:2n6: y = 0.02x − 40.45, 2 22:1n9* adjusted R2 = 0.06, SE = 0.53; 20:4n6: y = * 22:1n7* 0.02x − 33.51, adjusted R2 = 0.09, SE = 1 0.41; 22:5n6; y = 0.01x − 27.26, adjusted 2 R = 0.00, SE = 2.70), which was signifi- 0 cant for 3 of them (18:2n6: F1,186 = 12.13, * p < 0.001; 22:6n3: F = 4.15, p < 0.05; 1,186 –1 ln(% FA/18:0) 20:4n6:F1,186 =19.23,p<0.0001)(Fig.4).

–2 * Dive behaviour –3 1980 1985 1990 1995 2000 2005 2010 2015 The full factorial repeated-measures Year ANOVA on the number of dives >50 m Fig. 3. Correlation between the transformation (ln[% FA/18:0]) of each of the 5 made with respect to depth found a dietary fatty acids (FA) that are representative of Arctic cod over time with significant interaction between season least squares regression lines. *Significantly different at p < 0.01 and depth category (F5,1814 = 4.97, p < 0.001). Models for each depth category 2 found a significant effect of season for 18:2n6* 20:4n6* 0−25% depth (F2,403 = 6.33, p < 0.01), 1 * 22:5n6 26−50% (F2,438 = 8.10, p < 0.001), 51− − 22:6n3* 75% (F2,411 = 4.82, p < 0.01), and 76 0 * 100% (F2,451 = 3.43, p = 0.03) (Fig. 5A). There were significantly more dives –1 >50 m in autumn to 0−25% of total depth, and less dives in winter to 26− * –2 75% of total depth (Fig. 5A). More deep dives were made to 76−100% of ln(% FA/18:0) –3 total depth in winter compared to summer (Fig. 5A). The full factorial –4 repeated-measures ANOVA on the number of dives made to different –5 depth bins found a significant interac- 1980 1985 1990 1995 2000 2005 2010 2015 tion between season and depth cate- Year gory (F8,2440 = 19.24, p < 0.001). Models Fig. 4. Correlation between the transformation (ln[% FA/18:0]) of each of the 4 for each depth category found a signif- dietary fatty acids (FA) that are representative of capelin with least squares icant effect of season for all depths regression lines. *Significantly different at p < 0.05

(50−100 m: F2,406 = 23.50, p < 0.0001); 100−200 m: F2,272 = 10.76, p < 0.0001; 200−300 m: for 0−60 s (F1,122 = 7.14, p < 0.01), 61−180 s (F1,122 = F2,399 = 7.59, p < 0.001; 400−500 m: F2,406 = 30.42, p < 46.25, p < 0.0001), 181−360 s (F1,11 = 69.87, p < 0.0001; >500 m: F2,300 = 38.42, p < 0.0001), except 0.0001), 361−540 s (F1,106 = 22.54, p < 0.0001), 541− 300−400 m (F2,406 = 2.67, p = 0.07) (Fig. 5B). There 720 s (F1,118 = 51.28, p < 0.0001), 721−900 s (F1,121 = were significantly more dives to shallower depths in 432.06, p < 0.0001), and 901−1080 s (F1,115 = 326.66, summer (50−100 and 200−300 m) and significantly p < 0.0001) (Fig. 6). In general, short dives were more fewer dives to deep depths (400−500 and >500 m) frequent in summer and autumn compared to winter, compared to autumn and winter (Fig. 5B). while dives of longer duration were more prominent The full factorial repeated-measures ANOVA on in winter, with few of these dives made in summer number of dives of different durations found a signif- (Fig. 6). It was not possible to run simple effects mod- icant interaction between season and dive duration els for dive duration in the 1260, 1440, and >1440 s

(F3,1225 = 141.33, p < 0.0001). Models for each dive bins because in these cases only a few whales ever duration category found a significant effect of season made dives this long, and they were usually in 1 season 266 Endang Species Res 31: 259–270, 2016

Fig. 5. Mean number of dives (±SE) made to different depth categories for beluga whales from Cumberland Sound in summer (number of 6 h blocks collected = 232), autumn (n = 83), and winter (n = 208). (A) Number of dives >50 m deep in relation to bottom bathymetry. (B) Number of dives made to different programmed dive depth bins. *Levels of significance vary (see ‘Results’); least significance is p < 0.01; ϕ indicates a significant difference between winter and autumn, but no significant dif- ference between winter and summer, and δ indicates a significant difference between winter and summer, but no significant difference between winter and autumn. The range of depths encountered by beluga whales in each season is shown in the key, along with the average depth encountered

60 DISCUSSION Summer Autumn 50 Winter Beluga whales in Cumberland Sound have experi- enced a change in their fatty acid values since the 40 * 1980s and seem to have increased their consumption of capelin, while decreasing reliance on Arctic cod over the past 3 decades. Fatty acids in blubber repre- 30 sent diet over the previous few weeks (Kirsch et al. 2000, Iverson et al. 2004, Budge et al. 2006), and all No. of divesNo. 20 *** samples (except 5 that were collected in winter) used in this study were collected in summer (June to Sep- 10 *** tember); thus, fatty acids represent primarily a sum- * *** * mer diet signature for this group of whales. This sug- *** gests that capelin consumption in summer months 0 60 180 360 540 720 900 1080 1260 1440 >1440 has been increasing while cod consumption has been Dive duration (s) decreasing; however, explained variation was low. Fig. 6. Mean number of dives (±SE) made to different dive du- Stable isotopes, which represent diet integrated over ration categories for beluga whales from Cumberland Sound in summer (number of 6 h blocks collected = 360), autumn (n = a longer time span (2 to 3 mo for skin and several 146), and winter (n = 295). *Levels of significance vary (see months for muscle; St. Aubin et al. 1990, Sponheimer ‘Results’); least significance is p < 0.01 et al. 2006), in Cumberland Sound beluga skin and muscle have also changed since the 1980s, which (winter). For instance, only 1 whale (39323 = 10 dives) may be attributed to increasing capelin consumption made dives to the >1400 s (23 m) duration dive bin, (Marcoux et al. 2012). and these dives were only made in winter. Only 3 The primary fatty acids that distinguish Arctic cod whales (39296 = 5 dives, 39323 = 22 dives, and 57594 from capelin (Kelley et al. 2010) were evaluated to = 2 dives) made dives to the 1261−1400 s dive bin, all see specifically if the significant change in fatty acid in winter. Ten dives were made in autumn by 2 signatures from the 1980s could be attributed to whales (39323 = 6 dives and 57594 = 4 dives) to the changes in cod and capelin consumption; however, 1081−1260 s dive duration category, while 150 dives inferring diet from only a few fatty acids can be prob- were made to this category in winter by 4 whales lematic (Budge et al. 2006). Unfortunately, we did not (57594 = 18 dives, 39323 = 94 dives, 39308 = 10 dives, have fatty acid profiles from cod and capelin from and 39296 = 28 dives). Cumberland Sound for 1980 to 2010 to compare to Watt et al.: Cumberland Sound beluga diet and diving 267

the beluga values and obtain an estimate of cod and Petersen et al. 1986, Christiansen et al. 2012, Hauser capelin consumption. Although this would have been et al. 2015, Majewski et al. 2016). Capelin, on the ideal, it would have required a long-term monitoring other hand, are found in shallower waters, typically project in Cumberland Sound that began in the from 50 to 100 m in the Gulf of Alaska (Brown 2002), 1980s. As this was not possible, we believe it is useful and capelin found in stomachs of belugas from to at least investigate the fatty acids that seem to Alaska measured an average of 124 mm in length decipher Arctic cod from capelin, particularly since (Quakenbush et al. 2015). If this trend is the same for there is evidence that the 2 species make up the belugas in Cumberland Sound, dives from 50 to majority of summer diet for Cumberland Sound belu- 100 m were the most frequent type of deep dive and gas (Marcoux et al. 2012). The Arctic cod and capelin occurred primarily in the summer months, whereas samples collected by Kelley et al. (2010) came from deeper dives (300 to 400 m) occurred in all seasons. different locations: cod was collected in the high Arctic, This may suggest that capelin is dominating diet in while capelin was collected in Hudson Bay. In addi- the summer, while Arctic cod is more prevalent in the tion, explained variation was low and beluga metab- autumn and winter seasons. olism may affect fatty acids differently (Iverson et al. When dives were evaluated in relation to bottom 2004). As a result, the interpretation that there is an bathymetry, dives to the 76−100% category were still increasing trend in fatty acids distinctive for capelin the most prevalent in summer (although less common and that a decreasing trend is common in Arctic cod than in autumn or winter). Whales make most of their should be interpreted with caution; however, our dives in the summer at 50 to 400 m. As a result of the study does support a shift in the dietary fatty acid binning of the dive depths, a dive that fell into the profiles of beluga whales since the 1980s that is con- 100−200 m bin, for example, was counted as a 200 m current with an invasion of capelin in Cumberland dive for the purposes of confirming the number of Sound (Ulrich 2013). dives to the different categories of the water column. Our dive data represents information from only 7 Since the average summer depth is only 247 m, any beluga whales (1 tag lasting only 4 d) that were dive that fell in a bin deeper than 50−100 m would be tagged over 3 yr with males being tagged in only 1 of in the 76−100% category. Only those dives that fell those years. We are using these whales to represent a into the 50−100 m depth bin would fall into the other population that is much larger (~1150 individuals; 3 portions of the water column. The binning of the Marcoux et al. 2016), and although we can account dive data, as well as the uncertainty with the bottom for individual variability in dive behaviour by using a depths in this region, may be influencing how the nested statistical model, we were not able to evaluate dive behaviour distributes across the depth cate- differences owing to year or sex. As a result, we rec- gories; however, since larger capelin tend to school at ommend caution in interpreting the dive data while 50 to 100 m, and this is where the most dives are balancing the valuable insight provided by data that occurring based on the absolute dive depths, it is is logistically difficult and expensive to obtain. possible that belugas may be foraging on this newly Generally, it is difficult to decipher the importance available prey source. Belugas also seem to be diving of Arctic cod versus capelin in diet from dive behav- to depths of 100 to 400 m fairly frequently in summer, iour, as the 2 fish species have overlapping geo- which may also indicate some foraging on Arctic cod graphic distributions (Orlova et al. 2009), and unfor- at these depths and would be in line with the forag- tunately there is little information about the depths at ing results from stable isotopes (Marcoux et al. 2012). which Arctic cod and capelin distribute within Cum- The deepest dives (those 400 m and greater) were berland Sound, particularly as capelin is a relatively prevalent in autumn and winter, and belugas made new species in this ecosystem (Ulrich 2013). How- more dives to the 76−100% depth category and dives ever, there is data on the depth distribution of the 2 of longer duration in winter compared to summer or species in other areas in the Arctic and they are autumn. Greenland halibut has been found in the known to distribute at different depths. Arctic cod stomachs of beluga whales from Greenland (Heide- are considered a semi-pelagic species as young are Jørgensen & Teilmann 1994) and is a deep benthic found in the pelagic zone, but adults are found near species with adults (50 to 60 cm) found at depths of the bottom (Falk-Petersen et al. 1986, Majewski et al. be tween 800 and 1200 m in Cumberland Sound 2016). Belugas in the Canadian High Arctic typically (DFO 2008, Dennard et al. 2009, 2010). The program- select larger Arctic cod as prey (~180 to 200 mm) ming design of the tags used on belugas in Cumber- (Matley et al. 2015), and prey of this size class are land Sound from 2006 to 2008 did not allow us to sep- typically found at depths of 200 to 400 m (Falk- arate any dives >500 m, but it is un likely that whales 268 Endang Species Res 31: 259–270, 2016

would make such energetically expensive dives in December to April (Brown et al. 2014), but their the winter for any reason other than foraging. Unfor- movements may also reflect dietary needs, and a pos- tunately, fatty acids from this study and stable iso- sible candidate prey at this time is Greenland hal- topes from Marcoux et al. (2012) were not able to ibut. The commercial halibut fishery in Cumberland evaluate winter feeding, as samples were collected Sound currently operates in the winter season (Den- primarily in later summer months and thus did not nard et al. 2010) and thus may compete with beluga integrate winter diet; however, based on our dive whales for resources at this time. An understanding data, it does seem that dive behaviour supports for- of beluga diet and dive behaviour is needed to make aging on Greenland halibut, and future studies informed conservation targets for Cumberland would benefit from collecting beluga blubber sam- Sound belugas. Fatty acid data presented in our ples (e.g. biopsy) year round. study seem to be reflecting changes that have been Cumberland Sound is an important region for mar- documented in the Cumberland Sound food web, ine mammals and provides a number of resources to and dive behaviour indicates that winter foraging the community of Pangnirtung. Beluga whales are an may be particularly important for beluga whales. important part of this ecosystem and are currently a threatened species (COSEWIC 2004). Our study, as Acknowledgements. All work was conducted under DFO well as results from stable isotopes (Marcoux et al. Licence to Fish for Scientific Purposes, and prior approval 2012), suggests beluga whales are incorporating both was obtained from the Freshwater Institute Care Arctic cod and capelin in their diet, but summer capelin Committee (FWI-ACC-06-07-010, FWI-ACC-07-08-038, consumption may be increasing. A switch from Arctic FWI-ACC-08-09-008), and followed approved protocols. We thank the many dedicated people in the research field cod to capelin is likely inconsequential for the energy camps for their valuable assistance with the handling and budget of beluga whales, as both capelin and Arctic instrumenting of the beluga whales, and the Hunters and cod have high caloric values (Hop & Gjøsæter 2013); Trappers Organization in Pangnirtung, Nunavut, Canada, however, the energetic expense of capturing and for all of their support. Thank you also to the many people who assisted with lab work for fatty acid analysis, particu- handling a capelin versus an Arctic cod is unknown. larly B. Rosenberg. Thanks also to S. Luque for running state Generally, belugas seem to target larger, deeper Arc- space models on tag data. Thank you to 3 anonymous tic cod and smaller, shallower capelin (Falk-Petersen reviewers whose comments improved the final version of the et al. 1986, Brown 2002, Matley et al. 2015, Quaken- manuscript. Fisheries and Oceans Canada, NSERC, Species bush et al. 2015). Overall, deeper dives to catch cod at Risk, the Nunavut Wildlife Management Board, and Arc- ticNet provided funding. are energetically more expensive, but the payoff is large since these cod are larger in size, whereas catching smaller capelin in shallow waters requires a LITERATURE CITED lower energy input, but results in a lower payoff as Bailleul F, Lesage V, Power M, Doidge DW, Hammill MO the fish are smaller. Thus, it is difficult to determine (2012) Differences in diving and movement patterns of the impact a switch from capelin to Arctic cod would two groups of beluga whales in a changing Arctic envi- have on the energy budget of individual belugas, but ronment reveal discrete populations. Endang Species we would expect it to be inconsequential, particu- Res 17:27−41 Box GEP, Cox DR (1964) An analysis of transformations. 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Editorial responsibility: Louise Chilvers, Submitted: October 6, 2015; Accepted: August 18, 2016 Wellington, New Zealand Proofs received from author(s): November 1, 2016